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Evolution of Microtubule Organizing Centers Across the Tree of Eukaryotes

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Evolution of Microtubule Organizing Centers Across the Tree of Eukaryotes The Plant Journal (2013) 75, 230–244 doi: 10.1111/tpj.12145 A GLORIOUS HALF-CENTURY OF MICROTUBULES Evolution of microtubule organizing centers across the tree of eukaryotes Naoji Yubuki* and Brian S. Leander The Departments of Botany and Zoology, Beaty Biodiversity Research Centre and Museum, University of British Columbia, 6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada Received 16 December 2012; revised 04 February 2013; accepted 5 February 2013; published online 8 February 2013. *For correspondence (e-mail [email protected]). SUMMARY The architecture of eukaryotic cells is underpinned by complex arrrays of microtubules that stem from an organizing center, referred to as the MTOC. With few exceptions, MTOCs consist of two basal bodies that anchor flagellar axonemes and different configurations of microtubular roots. Variations in the structure of this cytoskeletal system, also referred to as the ‘flagellar apparatus’, reflect phylogenetic relationships and provide compelling evidence for inferring the overall tree of eukaryotes. However, reconstructions and sub- sequent comparisons of the flagellar apparatus are challenging, because these studies require sophisticated microscopy, spatial reasoning and detailed terminology. In an attempt to understand the unifying features of MTOCs and broad patterns of cytoskeletal homology across the tree of eukaryotes, we present a compre- hensive overview of the eukaryotic flagellar apparatus within a modern molecular phylogenetic context. Specifically, we used the known cytoskeletal diversity within major groups of eukaryotes to infer the unifying features (ancestral states) for the flagellar apparatus in the Plantae, Opisthokonta, Amoebozoa, Stramenopiles, Alveolata, Rhizaria, Excavata, Cryptophyta, Haptophyta, Apusozoa, Breviata and Collodictyo- nidae. We then mapped these data onto the tree of eukaryotes in order to trace broad patterns of trait changes during the evolutionary history of the flagellar apparatus. This synthesis suggests that: (i) the most recent ancestor of all eukaryotes already had a complex flagellar apparatus, (ii) homologous traits associ- ated with the flagellar apparatus have a punctate distribution across the tree of eukaryotes, and (iii) stream- lining (trait losses) of the ancestral flagellar apparatus occurred several times independently in eukaryotes. Keywords: biodiversity, cytoskeleton, evolution, excavates, flagellar apparatus, protists. Apusozoa, Breviata, Collodictyonidae, Cryptophyta and A BRIEF OVERVIEW OF EUKARYOTIC DIVERSITY Haptophyta) and five major clades or ‘supergroups’ [the Eukaryotes that are not plants, animals or fungi, the so- Plantae, Opisthokonta, Amoebozoa, SAR (Stramenopiles, called ‘protists’, are much more diverse than is usually Alveolata and Rhizaria) and Excavata] (Kim et al., 2006; appreciated, particularly in regard to total species numbers Burki et al., 2009; Roger and Simpson, 2009; Ishida et al., and the ultrastructural and genomic complexity of their 2010; Parfrey et al., 2010; Heiss et al., 2011; Adl et al., 2012; cells (Ishida et al., 2010; Parfrey et al., 2010; Adl et al., Zhao et al., 2012). 2012). A comprehensive tree of eukaryotes with resolved Land plants, animals and fungi are each most closely phylogenetic relationships among dozens of very different related to different lineages of single-celled eukaryotes, lineages is beginning to emerge through the rapid accumu- and are nested within different supergroups. For instance, lation and comparative analysis of genomic data (e.g., land plants are nested within the Plantae, which also Parfrey et al., 2010; Burki et al., 2012; Brown et al.,2012).This includes red algae, green algae and glaucophytes (Graham phylogenetic context provides the foundation for inferences and Wilcox, 2000; Archibald and Keeling, 2004) (Figures about the evolution of the eukaryotic cytoskeleton. The 1a–c). Members of this supergroup possess plastids that most widely accepted tree of eukaryotes currently consists were derived directly from a cyanobacterium via (primary) of several minor groups, without a clear sister lineage (the endosymbiosis; glaucophytes still possess a cyanobacterial 230 © 2013 The Authors The Plant Journal © 2013 John Wiley & Sons Ltd Macroevolution of microtubule organizing centers 231 Figure 1. Images representing major lineages of eukaryotes. Some photos are modified with (a) (b) (c) permission from Micro*scope (c, g, h, k): (a) Marchantiophyta, Conocephalum; (b) Rhodophyta, Phacelocarpus; (c) Glaucophyta, Cyanophora; (d) Scyphozoa, Chrysaora; (e) Choanoflagellata (f) Fungi, Agaricus; (g) Myxogastria, Dydimium (‘Hyperamoeba’); (h) Archeamoeba, Mastigina; (i) Myxogastria, Physarum; (d) (e) (f) (j) Stramenopile, Mallomonas; (k) Dinoflagellate, Polykrikos; (l) Rhizaria, Calcarina; (m) Metamonada, Trichonympha; (n) Discoba, Rapaza. (o) Metamonada, Kipferlia; (p) Cryptophyta, Chroomonas; (q) Cryptophyta, Cryptomonas; (r) Haptophyta, Gephyrocapsa. (g) (h) (i) (j) (k) (l) (m) (n) (o) (p) (q) (r) cell wall around their plastids (Aitken and Stanier, 1979; tains a diverse assemblage of amoeboflagellates and slime Scott et al., 1984). Animals and fungi are both nested molds (Watkins and Gray, 2008; Shadwick et al., 2009) (Fig- within the Opisthokonta, which also includes choanoflagel- ures 1g–i). The Apusozoa branches as the nearest sister lates and chytrids, among other lineages (Lang et al., 2002) group to a clade consisting of the Opisthokonta and (Figures 1d–f). Most species in this supergroup possess a Amoebozoa (a clade that was once recognized as ‘uni- posterior flagellum that undulates to push the cell konts’; Kim et al., 2006; Cavalier-Smith and Chao, 2010). forwards (Cavalier-Smith and Chao, 2003a). The nearest Most of the supergroups also contain representatives of sister group to opisthokonts is the Amoebozoa, which con- what are arguably the three most dissimilar modes of © 2013 The Authors The Plant Journal © 2013 John Wiley & Sons Ltd, The Plant Journal, (2013), 75, 230–244 232 Naoji Yubuki and Brian S. Leander (eukaryotic) life on the planet: photoautotrophs, predators images of eukaryotic cells were taken with a transmission and parasites. For instance, the SAR clade contains plant-like electron microscope in the 1960s. The most recent review kelps and diatoms, saprophytic water molds (oomycetes), of the eukaryotic flagellar apparatus in microalgae was filter-feeding radiolarians, predatory ciliates and the notori- published more than a decade ago (Moestrup, 2000); how- ous blood-born parasite Plasmodium (Patterson, 1989; Cava- ever, a lot has changed since then, especially knowledge lier-Smith and Chao, 2003b; Leander and Keeling, 2003; about new lineages of eukaryotic cells and where they fit Roger and Simpson, 2009; Burki et al., 2010; Parfrey et al., into the overall tree of eukaryotes. In an attempt to under- 2010) (Figures 1j–l). The Excavata contains photosynthetic stand broad patterns of cytoskeletal homology in eukary- Euglena and relatives, the diarrhea-causing parasite Giardia, otes, we present a relatively comprehensive overview and several other different lineages of parasites and free-liv- of the eukaryotic flagellar apparatus within a modern ing phagotrophs (Figures 1m–o). There is still debate as to molecular phylogenetic context. We address the known whether or not the Excavata is monophyletic (a group that cytoskeletal diversity within the major groups of eukary- consists of an ancestor and all of its descendants), an infer- otes introduced above in order to infer ancestral traits and ence that happens to be crucial for understanding the origin subsequent trait changes during the evolutionary history and evolution of the eukaryotic cytoskeleton (Simpson and of the flagellar apparatus. Roger, 2004; Simpson et al., 2006). The synthesis of cyto- The eukaryotic flagellar apparatus is almost always com- skeletal traits we provide below suggests that the Excavata posed of two (or more) basal bodies that anchor the axo- is not monophyletic and instead represents a (paraphyletic) nemes, if present, and different microtubular roots; the stem group from which all other eukaryotes evolved. system functions as the MTOC for the entire eukaryotic cell (Moestrup, 1982; Sleigh, 1988; Andersen et al., 1991; Beech FUNDAMENTAL FEATURES OF MTOCS: THE FLAGELLAR et al., 1991; Moestrup, 2000) (Figure 2). The flagellar appa- APPARATUS ratus is therefore a complex ultrastructural system in Comparative morphology of the microtubular cytoskeleton almost every eukaryotic cell, and plays vital roles in a in eukaryotes started at about the same time the first variety of cell functions, such as locomotion, feeding (a) (b) (c) (d) (e) Figure 2. Transmission electron microscopy (TEM) sections showing the divesity and major components of the flagellar apparatus in five representive lineages of eukaryotes: (a) Plantae, Pyramimonas (‘Prasinophyta’), modified with permission from Hori and Moestrup (1987); (b) Stramenopile, Apoikia (Stramenopile); (c) Excavata, Uteronympha (Metamonada), modified with permission from Brugerolle (2006b); (d) Haptophyta, Pleurochrysis, modified with permission from Inouye and Pienaar (1985); (e) Collodictyonidae, Collodictyon, modified with permission from Brugerolle et al. (2002). Scale bars: (a, b, d, e) 200 nm; (c) 400 nm. © 2013 The Authors The Plant Journal © 2013 John Wiley & Sons Ltd, The Plant Journal, (2013), 75, 230–244 Macroevolution of microtubule organizing centers 233 (phagocytosis), and the formation of microtubular arrays THE DIVERSITY OF MTOCS REFLECTS THE
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